TrmB1, a novel nucleoid-associated protein orchestrates dynamic chromatin organization and cell cycle progression in archaea

Archaea of the order Sulfolobales have a eukaryotic-like cell cycle but lack histone-like proteins; therefore, how the chromatin organization in these archaea changes and dynamically regulates cell cycle progression remains a puzzle. Here, we identify a novel nucleoid-associated protein (NAP), SisTrmB1, as a central player in these processes in Saccharolobus islanidicus. Its gene is essential for cell viability and is transcribed in a cell cycle-dependent manner. ChIP-seq analysis reveals that SisTrmB1, which exhibits DNA-bridging activity, binds to genome-wide DNA with a preference for AT-rich sequences with a higher enrichment at transcription start sites (TSS). Hi-C analysis reveals global changes in chromatin interaction patterns between the lowest and highest transcription levels of sistrmB1 in synchronized cells. Overexpression of SisTrmB1 results in cell cycle arrest at G2-phase and disrupts global transcription pattern. Interestingly, the global chromatin interaction changes (Hi-C) brought about by SisTrmB1 overexpression mirror those observed in synchronized cells. These results strongly suggest that cell cycle-coordinated chromatin compartment remodeling is associated with SisTrmB1 expression. Our study provides insights into how the dynamic organization of chromosome affects cell cycle-dependent global transcription in Sulfolobales archaea.